Alpha-synuclein (aS) is a small presynaptic protein implicated in the pathogenesis of Parkinsons disease. It partitions between an intrinsically disordered cytosolic state and a more structured vesicle-bound state. Structural studies of &#945;S have, to date, been based largely on the SDS detergent-bound conditions, for which &#945;S displays &#945;-helices in the N-terminal domain and an unstructured C-terminal tail that remains free in solution. We have investigated the structure and biophysics of &#945;S in the presence of lipid bicelles. Lipid bicelles offer the advantage of a natural lipid bilayer while also featuring small vesicle radii which render them amenable to solution NMR studies. Our biophysical and NMR data show that &#945;S displays a preference for specific combinations of acidic and zwitterionic lipid headgroups and give evidence that &#945;S participates in dynamic exchange processes on the lipid bilayer that may reorganize the bilayer with time. Additionally, our results show that this lipid interaction of &#945;S is coupled with effects on aggregation propensity. For full length &#945;S, lipid bicelles greatly enhance aggregation, producing well-ordered, fibrillar structures. The lipid-induced aggregation is even more strongly stimulated for a C-terminal deletion construct of &#945;-synuclein.